Increasing Mastectomy Rates Among all Age Groups for Early Stage Breast Cancer: A 10-Year Study of Surgical Choice
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ORIGINAL ARTICLE Increasing Mastectomy Rates Among all Age Groups for Early Stage Breast Cancer: A 10-Year Study of Surgical Choice Anthony E. Dragun, MD,* Bin Huang, Dr PH, MS, ,à Thomas C. Tucker, PhD, MPH,à and William J. Spanos, MD* *Department of Radiation Oncology, James Graham Brown Cancer Center, University of Louisville School of Medicine, Louisville, Kentucky; Department of Biostatistics, College of Public Health, University of Kentucky, Lexington, Kentucky; and àKentucky Cancer Registry, Markey Cancer Center, University of Kentucky, Lexington, Kentucky n Abstract: First-line surgical options for early stage breast cancer and ductal carcinoma in situ include breast conserv- ing surgery or mastectomy. We analyzed factors that influence the receipt of mastectomy and resultant trends over time. Registry analysis was carried out for 21,869 women who underwent up-front surgical treatment for stage 0, I or II breast cancer between 1998 and 2007 using data from the Kentucky Cancer Registry. We examined the trend of treatment over time and assessed the probability of receiving mastectomy using multivariate logistic regression. Overall, 54.5% of women received breast conservation and 45.5% received mastectomy over a 10-year period (annual BCS rate range: 46.9–61.2%). The overall mastectomy rate substantially decreased from 53.1% in 1998 to 38.8% in 2005 (p < 0.0001), but then increased to 45% in 2007 (p < 0.001). Between 2005 and 2007, the increase in mastectomies in the age groups of
Mastectomy Rates Rising for all Ages • 319 breast cancer screening and public awareness cam- was 20 years old or older; the cancer was the first pri- paigns have resulted in earlier detection of more mary cancer diagnosed; only AJCC stage 0 (ductal favorable disease, a paradoxical recent trend toward carcinoma in situ), Stage I and II cases included. Cases more extensive surgical management has been abstracted from autopsy or death certificate only were observed (5,7,17,20–23). There is currently a debate excluded. over whether the reports of increasing mastectomy use The KCR is a population-based registry, and has are isolated only to individual treatment centers been awarded the highest level of certification by the (7,17,21,23,24), as larger, population-based studies North American Association of Central Cancer have failed to show the same trend (5). Registries for an objective evaluation of completeness, During the last few decades, major cancer centers accuracy, and timeliness every year since 1997. The in large cities have paved way for significant growth KCR is also part of the Surveillance, Epidemiology, and spread of multidisciplinary breast cancer care and End Results (SEER) program, which is considered with access to specialized breast surgeons coupled one of the most accurate and complete population- with integration of adjuvant local and systemic thera- based cancer registries in the world. The KCR also pies. In the US, approximately 80% of the population links its database annually with the National Death lives in or near a major metropolitan center and thus Index (NDI) to capture the most accurate survival the aforementioned studies are heavily influenced by information. the inclusion of significant numbers of urban patients For purposes of this analysis, the treatment is cate- (25). In fact, subset analyses of nearly all national gorized into two groups: Mastectomy or BCS. Mastec- database studies on this subject indicate that the low- tomy is defined as modified radical mastectomy, total est relative rates of BCS exist in more sparsely popu- mastectomy or simple mastectomy. BCS is defined as lated regions, especially the South and ⁄ or Southeast any surgery less than the aforementioned, including (6,8,10,12,14,16,18,19,26–28). partial mastectomy (with or without nipple resection), The Commonwealth of Kentucky does not encom- segmental mastectomy, lumpectomy, tylectomy, quad- pass a city listed among the top 25 incorporated enti- rantectomy or re-excision of the biopsy site for gross ties (according to the United States Census Bureau) nor or microscopic residual disease. a top 40 metropolitan statistical area (as defined by the Race, age at diagnosis, urban ⁄ rural status and United States Office of Management and Budget). In Appalachian status are primary demographic interests addition, Kentucky does not contain a National Cancer of the study. Urban ⁄ Rural status was based on the Institute (NCI) designated cancer center. The purpose 2003 Urban-Rural Continuum codes with 1–3 defined of this study was to quantify the rate of BCS for pre- as urban and 4–9 as rural. The county-level Appala- invasive and early stage breast cancer in this under- chian status was based on definitions by the Appala- served southern state, and to identify determinants of chia Regional Commission. Other demographical and mastectomy along with trends over time. clinical variables included in the study were year at diagnosis, smoking history, insurance status, survival status at the end of the study, primary cancer METHODS sequence number, laterality, stage, nodes examined, This retrospective population-based registry study ER ⁄ PR status, tumor grade, histology, and tumor size. was approved by the institutional review board at the The descriptive analysis for demographics and clini- University of Louisville School of Medicine. The study cal factors was performed. We used chi-squared tests concept, design, and completion represents a collabo- to examine associations between treatment and vari- rative effort between investigators at the University of ables described above. Multivariate logistic regressions Louisville’s James Graham Brown Cancer Center were fitted to evaluate the association between mastec- (Louisville, KY) and the Kentucky Cancer Registry at tomy utilization and age at diagnosis ⁄ race ⁄ residence the University of Kentucky’s Markey Cancer Center location while controlling for other covariates. The (Lexington, KY). Data for female-only breast cancer final model included only covariates with a signifi- cases diagnosed between 1998 and 2007 were cance level of 0.05 or less. Model goodness of fit, mul- obtained from the Kentucky Cancer Registry (KCR). ticollinearity, and interactions were also examined. All The study included 21,869 women who met the analyses were done using SAS Statistical software following inclusion criteria: age at cancer diagnosis version 9.1 (Cary, NC, USA). All statistical tests were
320 • dragun et al. two sided with a p-value £ 0.05 used to identify statis- Table 1. Demographics, Disease Characteristics, tical significance. and Surgical Details for all Cases Included in this Study (N = 21,869) Variable N % RESULTS Age at diagnosis The study cohort consisted of 21,869 patients who
Mastectomy Rates Rising for all Ages • 321 Table 1. (Continued ) (a) Age < 50 years 70.0% Variable N % 60.0% Axillary dissection 10,894 49.8 50.0% Not specified 341 1.6 Primary surgical choice 40.0% BCS 11,919 54.5 Mastectomy 9950 45.5 30.0% 20.0% Surgical Choice by Year 10.0% 2500 0.0% 1998 1999 2000 2001 2002 2003 2004 2005 2006 2007 2000 BCS Mastectomy 1500 (b) Age 50-69 years # Casess 70.0% 1000 60.0% 50.0% 500 40.0% 0 30.0% 1998 1999 2000 2001 2002 2003 2004 2005 2006 2007 Mastectomy 1114 1165 1069 1143 1064 854 841 814 892 999 BCS 984 1115 1119 1188 1214 1249 1245 1286 1295 1219 20.0% 10.0% Figure 1. Annual relative rates of primary surgical choice (BCS versus mastectomy) for all cases of stage 0, I, and II breast cancer 0.0% from 1998–2007 in the Commonwealth of Kentucky. 1998 1999 2000 2001 2002 2003 2004 2005 2006 2007 BCS Mastectomy specifics, patients were more likely to receive a mas- (c) Age ≥ 70 years tectomy if they had stage II disease (p < 0.0001), 70.0% poorly differentiated tumors(p < 0.0001), lobular can- 60.0% cers(p < 0.0001), and hormone receptor negative dis- ease (p < 0.0001). Larger tumor size and more 50.0% extensive axillary surgery were associated with higher 40.0% likelihood of receiving a mastectomy (p < 0.0001). 30.0% Table 3 shows the results of multivariate analysis including the entire list of variables included in 20.0% Tables 1 and 2. The most significant independent 10.0% demographic factors associated with receipt of mastec- 0 0% 0.0% tomy were, lack of private insurance (p < 0.0001), fol- 1998 1999 2000 2001 2002 2003 2004 2005 2006 2007 lowed by rural county of residence (p = 0.0187), and BCS Mastectomy advanced age (p = 0.0332). With regard to disease Figure 2. (a–c): Surgical choice by age over the decade of the specifics, mastectomy was more likely to be adminis- study period for women (a)
322 • dragun et al. Table 2. Univariate Analysis for the Association Table 2. (Continued ) of Demographic and Disease Factors with Pri- mary Surgical Choice for all Cases Included in Primary surgical choice this Study (N = 21,869) BCS Mastectomy Primary surgical choice Variables N % N % p-value BCS Mastectomy 3.1–4.0 388 29.2 939 70.8 >4.0 243 24.0 768 76.0 Variables N % N % p-value Not specified 1225 59.0 852 41.0 Lymph node surgery Age at diagnosis None 3399 75.7 1093 24.3
Mastectomy Rates Rising for all Ages • 323 cal strategies have had a long evolution over more In a retrospective review of a prospective collective than 50 years, it was the publication of the 1991 NIH database between 1994 and 2007 at the Moffitt consensus conference on the treatment of patients Cancer Center, mastectomy rates were shown to with early stage breast cancer that ushered in this so- decrease between 1994 and 2004 and then signifi- called ‘‘post-mastectomy’’ era (4). Indeed, prior to the cantly increase from 2004 to 2007 (from 44% to NIH consensus, only about 35% of women with Stage 60%) (23). Mastectomy was correlated with younger I and 19% of women with stage II breast cancer age, increasing tumor size, and presence of lympho- nationwide underwent BCS, however, by 1995, these vascular invasion, but the major determining factor national numbers increased to approximately 60% was the year of diagnosis with the highest odds ratio and 40%, respectively (6). of mastectomy as seen between 2004 and 2007 (23). Despite this sea change, broad discrepancies in the A regional study from the California Cancer Registry application of BCS versus mastectomy have been showed the recently observed shift away from BCS observed based on patient demographic and disease- back to mastectomy beginning around the year 2000, specific characteristics. The mastectomy rate has been and most notable for younger, non-Hispanic White correlated with factors such as age, lymph node status, women of high socio-economic status (22). poverty level, educational level, and even widowed Explanations for these recent trends range from status (7,18). But perhaps most often, mastectomies changing patient attitudes, better surgical techniques, have been unevenly distributed geographically, with and access to more treatment choices as well as the highest in the south region compared to regions in increasing perception about future risks of in breast the northeast and west coast (6,18). Furthermore, tumor recurrence and contralateral tumor recurrences rural residency designation, even within a region with (21). Another explanation for rising mastectomy rates high rates of BCS, also predicts for receipt of mastec- has been the increased use of preoperative MRI. tomy (8,15). A SEER study of surgical choice in A study of over 5,000 patients from the Mayo Clinic women from 1992–1993 showed that rural residency identified breast MRI as a major independent predic- was an independent factor affecting the receipt of tive factor of mastectomy (odds ratio = 1.7) for mastectomy with an odds ratio of 1.58, with an over- patients who underwent surgery between 1997 and all mastectomy rate of rural patients in the study of 2006. However, mastectomy rates also increased in 59.9 versus 44.9 for non rural patients (15). In a study the same series from 2004 to 2006 among patients of the New Hampshire Cancer Registry from 1998 to who did not undergo an MRI and thus surgical year 2000, women were more likely to have a mastectomy was an independent predictor for mastectomy (24). if they lived greater than or equal to 20 miles from a The interest generated by the corroborating studies radiation therapy facility or if their diagnosis was from multiple institutions recently led to a large popu- made in the wintertime when daily travel for radiation lation-based (SEER) study conducted by Haberman therapy after BCS would entail more inconvenience or et al. (5). In this nationwide analysis of over 200,000 hazard (8). patients who underwent surgery between 2000 and Additional factors play into surgical choice, for 2006 the overall mastectomy rate decreased from even when BCS is desired by the patient, it may not approximately 41% to 37% (5). However, the same be advisable (16). A large study performed at the study noted that although the rate of unilateral mas- University of Michigan specifically quantified the fact tectomy had decreased the rate of contralateral pro- that although most women with early stage breast phylactic mastectomy had substantially increased (5). cancer may be considered good candidates for BCS in Although it may appear at first glance that the conclu- general, approximately one third are ultimately con- sions of this SEER study directly contradict those of sidered poor candidates secondary to issues related to the aforementioned single institutions, in fact both tumor size to breast size ratio or other reasons such as observations may be valid. diffuse microcalcifications on mammography (17). Our current study is in agreement with the national Even so, the reason most often cited for the choice SEER registry, showing that the absolute mastectomy of mastectomy in breast conservation candidates is rate is lower than it was compared to a decade ago by patient choice, and despite better screening, earlier approximately the same magnitude (53.1% in 1998 detection, and patient selection, women seem to be versus 45.0% in 2007). However, when looking choosing mastectomy in larger numbers (17,21–24). specifically at the last 3–4 years of the analysis—the
324 • dragun et al. same time period of the above-mentioned single insti- must be targeted to these underserved populations to tution series—the trend in the use of mastectomy is improve treatment choice and access for vulnerable unmistakably upward. Moreover, our data suggest patient populations. Additional study is warranted to that this trend is present throughout all age groups quantify additional factors that underlie this surgical with absolute increase in mastectomy use of approxi- trend in non-underserved populations. mately 5–8%. Surprisingly, this trend is observed even among the elderly, in whom radical surgery is poten- tially more risky and partial mastectomy alone with- SUPPORT ⁄ CONFLICTS OF INTEREST out the addition of radiotherapy has become a more There was no financial support in the conception, widely accepted option (29). Our data are confirma- design or completion of this study. There are no con- tory of other studies, reinforcing that the dispropor- flicts of interest to disclose by any of the authors. tionate use of mastectomy remains a problem for the uninsured or underinsured, rural and elderly patients, all of whom may lack sufficient access to multidisci- REFERENCES plinary breast care. 1. Fisher B, Jeong JH, Anderson S, Bryant J, Fisher ER, The strength of our study lies in the ability of the Wolmark N. Twenty-five-year follow-up of a randomized trial com- paring radical mastectomy, total mastectomy, and total mastectomy Kentucky Cancer Registry to represent a large cross followed by irradiation. N Engl J Med 2002;347:567–75. section of academic and community centers within an 2. van Dongen JA, Voogd AC, Fentiman IS, et al. 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